The wheat clock strikes a balance across subgenomes to regulate gene expression

Increasing crop yields is complicated by the polyploid nature of our major crops. A recent PLOS Biology study provides a transcriptomic view of the influence of the circadian clock on regulating agriculturally relevant traits in the polyploid bread wheat.

each subgenome (A, B, and D) into a circadian clock with control over critical physiological processes like the distantly related Arabidopsis clock (Fig 1).
With 51.7% of genes present in 3 copies (triads) in T. aestivum, Rees and colleagues tested whether there was evidence of 1 subgenome clock being more transcriptionally active or having unique circadian properties. A previous study in wheat found that 72% of triads had equivalent transcript abundance levels or were "balanced" [9]. Rees and colleagues performed a circadian time course RNA-sequencing experiment under constant light and temperature where rhythms in gene expression are driven solely by the clock. Rhythmicity analysis identified significantly rhythmic genes and assigned period (time between peaks), phase (time of peak), and amplitude values. Circadian imbalance was classified based on differences in these parameters for each triad. For the 16,359 expressed triads, more than 3 times as many were imbalanced as balanced, with rhythmicity accounting for the most variation. Interestingly, when assessing imbalance on the expression level as done previously [9], the level of imbalance changed depending on the time point emphasizing the importance of studying expression dynamics over time. It should be noted that these 2 studies were done in 2 different cultivars of wheat. Unique to the balanced triads was overrepresentation of gene functions related to photosynthesis and metabolic energy generation, which were also found among B. rapa paralogs with similar circadian expression pattern [10].
Consistent with studies in B. rapa [10], the balanced rhythmic triads were expressed at uniformly higher levels than even the highest expressed imbalanced triads, suggesting that all subgenome copies are contributing to clock function. A thorough comparison of circadian clock gene expression between wheat and Arabidopsis revealed most genes maintained a similar phase although they varied in period length. Gene coexpression networks were constructed to identify modules, or clusters of genes with similar expression patterns. Correlated modules with similar phase shared more Gene Ontology (GO) terms in common than modules that were out of phase.
Among all rhythmic genes between Arabidopsis and wheat, photosynthesis, response to abiotic stress, and macromolecule biosynthesis were enriched, supporting the evolutionary conservation of clock-controlled functions. These traits are especially relevant for current wheat breeding efforts that prioritize increasing photosynthetic capacity, yield, and stress tolerance [3,8]. For each of these pathways, examples could be found where specific genes had conserved phasing of expression in wheat and Arabidopsis, and examples of unique phasing of certain wheat homeologs, highlighting differences in circadian control (Fig 1). A pathway exhibiting more diverged clock regulation was starch metabolism, a process that is critical for plant growth [11]. In Arabidopsis and wheat, starch accumulates during the day and is degraded at night at a rate that is dependent on the length of the night [11,12]. In Arabidopsis, this process is clock controlled [11], and genes involved in starch biosynthesis and catabolism are circadian regulated. In wheat, there was much more variation in rhythmicity and phasing for genes in both the biosynthesis and catabolic steps including loss of rhythmicity for many homeologs suggesting that there is less constraint at the transcript level. Whether the proteins are rhythmic or this indicates less circadian control of this pathway is unknown.
Rees and colleagues provide new insight into the complexities of circadian regulation in an allopolyploid crop. This represents just 1 cultivar within T. aestivum, a crop that is grown between 67˚N and 45˚S with more than 560,000 cultivars adapted to different environmental regions that include winter and spring types [13]. How have their circadian networks been shaped to accommodate such wide geographic ranges? Based on studies in tomato, soybean, and barley, we can expect to find variation in circadian properties across latitudinal clines [3]. If this holds true in wheat, are the circadian imbalanced and balanced triads conserved across the species or do we see intraspecific variation in the subgenome contributions to the circadian network? Additional time course datasets across diverse cultivars will be critical to identifying targets specific to the geographical location and in developing models to predict what effect integrating new traits will have on the underlying circadian network. If the 140 million-year conservation of clock control over these critical biological processes has taught us anything, it is that we can no longer ignore the clock.